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The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates.

ABSTRACT: Ascidians are the closest living relatives of vertebrates, and their study is important for understanding the evolutionary processes of oocyte maturation and ovulation. In this study, we first examined the ovulation of Ciona intestinalis Type A by monitoring follicle rupture in vitro, identifying a novel mechanism of neuropeptidergic regulation of oocyte maturation and ovulation. Ciona vasopressin family peptide (CiVP) directly upregulated the phosphorylation of extracellular signal-regulated kinase (CiErk1/2) via its receptor. CiVP ultimately activated a maturation-promoting factor, leading to oocyte maturation via germinal vesicle breakdown. CiErk1/2 also induced expression of matrix metalloproteinase (CiMMP2/9/13) in the oocyte, resulting in collagen degradation in the outer follicular cell layer and liberation of fertile oocytes from the ovary. This is the first demonstration of essential pathways regulating oocyte maturation and ovulation in ascidians and will facilitate investigations of the evolutionary process of peptidergic regulation of oocyte maturation and ovulation throughout the phylum Chordata.

SUBMITTER: Matsubara S

PROVIDER: S-EPMC6786877 | biostudies-literature | 2019 Oct

REPOSITORIES: biostudies-literature

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The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates.

Matsubara Shin S Shiraishi Akira A Osugi Tomohiro T Kawada Tsuyoshi T Satake Honoo H

eLife 20191001

Ascidians are the closest living relatives of vertebrates, and their study is important for understanding the evolutionary processes of oocyte maturation and ovulation. In this study, we first examined the ovulation of <i>Ciona intestinalis</i> Type A by monitoring follicle rupture in vitro, identifying a novel mechanism of neuropeptidergic regulation of oocyte maturation and ovulation. <i>Ciona</i> vasopressin family peptide (CiVP) directly upregulated the phosphorylation of extracellular signa ...[more]

PMID: 31573508

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Project description:The central roles of luteinizing hormone (LH), progestin and their receptors for initiating ovulation have been well established. However, signaling pathways and downstream targets such as proteases that are essential for the rupture of follicular cells are still unclear. Recently, we found anovulation in nuclear progestin receptor (Pgr) knockout (Pgr-KO) zebrafish, which offers a new model for examining genes and pathways that are important for ovulation and fertility. In this study, we examined expression of all transcripts using RNA-Seq in preovulatory follicular cells collected following the final oocyte maturation, but prior to ovulation, from wild-type (WT) or Pgr-KO fish. Differential expression analysis revealed 3567 genes significantly differentially expressed between WT and Pgr-KO fish (fold change?2, p<0.05). Among those, 1543 gene transcripts were significantly more expressed, while 2024 genes were significantly less expressed, in WT than those in Pgr-KO. We then retrieved and compared transcriptional data from online databases and further identified 661 conserved genes in fish, mice, and humans that showed similar levels of high (283 genes) or low (387) expression in animals that were ovulating compared to those with no ovulation. For the first time, ovulatory genes and their involved biological processes and pathways were also visualized using Enrichment Map and Cytoscape. Intriguingly, enrichment analysis indicated that the genes with higher expression were involved in multiple ovulatory pathways and processes such as inflammatory response, angiogenesis, cytokine production, cell migration, chemotaxis, MAPK, focal adhesion, and cytoskeleton reorganization. In contrast, the genes with lower expression were mainly involved in DNA replication, DNA repair, DNA methylation, RNA processing, telomere maintenance, spindle assembling, nuclear acid transport, catabolic processes, and nuclear and cell division. Our results indicate that a large set of genes (>3000) is differentially regulated in the follicular cells in zebrafish prior to ovulation, terminating programs such as growth and proliferation, and beginning processes including the inflammatory response and apoptosis. Further studies are required to establish relationships among these genes and an ovulatory circuit in the zebrafish model.

Project description:BACKGROUND: The hormonal control of oocyte maturation and ovulation as well as the molecular mechanisms of nuclear maturation have been thoroughly studied in fish. In contrast, the other molecular events occurring in the ovary during post-vitellogenesis have received far less attention. METHODS: Nylon microarrays displaying 9152 rainbow trout cDNAs were hybridized using RNA samples originating from ovarian tissue collected during late vitellogenesis, post-vitellogenesis and oocyte maturation. Differentially expressed genes were identified using a statistical analysis. A supervised clustering analysis was performed using only differentially expressed genes in order to identify gene clusters exhibiting similar expression profiles. In addition, specific genes were selected and their preovulatory ovarian expression was analyzed using real-time PCR. RESULTS: From the statistical analysis, 310 differentially expressed genes were identified. Among those genes, 90 were up-regulated at the time of oocyte maturation while 220 exhibited an opposite pattern. After clustering analysis, 90 clones belonging to 3 gene clusters exhibiting the most remarkable expression patterns were kept for further analysis. Using real-time PCR analysis, we observed a strong up-regulation of ion and water transport genes such as aquaporin 4 (aqp4) and pendrin (slc26). In addition, a dramatic up-regulation of vasotocin (avt) gene was observed. Furthermore, angiotensin-converting-enzyme 2 (ace2), coagulation factor V (cf5), adam 22, and the chemokine cxcl14 genes exhibited a sharp up-regulation at the time of oocyte maturation. Finally, ovarian aromatase (cyp19a1) exhibited a dramatic down-regulation over the post-vitellogenic period while a down-regulation of Cytidine monophosphate-N-acetylneuraminic acid hydroxylase (cmah) was observed at the time of oocyte maturation. CONCLUSION: We showed the over or under expression of more that 300 genes, most of them being previously unstudied or unknown in the fish preovulatory ovary. Our data confirmed the down-regulation of estrogen synthesis genes during the preovulatory period. In addition, the strong up-regulation of aqp4 and slc26 genes prior to ovulation suggests their participation in the oocyte hydration process occurring at that time. Furthermore, among the most up-regulated clones, several genes such as cxcl14, ace2, adam22, cf5 have pro-inflammatory, vasodilatory, proteolytics and coagulatory functions. The identity and expression patterns of those genes support the theory comparing ovulation to an inflammatory-like reaction.

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The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates.

Publications

The regulation of oocyte maturation and ovulation in the closest sister group of vertebrates.

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